Neuroethology of male courtship in Drosophila: From the gene to behavior

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 200, Issue 4, 2014, Pages 251-264

  Yamamoto, Daisuke ^a   Sato, Kosei ^a   Koganezawa, Masayuki ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

Chromatin; fruitless; Identified neurons; Pheromones; Sexual dimorphism

Indexed keywords

DROSOPHILA PROTEIN; FRU PROTEIN, DROSOPHILA; NERVE PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL; COURTSHIP; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENETICS; MALE; METABOLISM; NERVE CELL; NERVE TRACT; PHYSIOLOGY; SEXUAL BEHAVIOR;

ANIMALS; COURTSHIP; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION; MALE; NERVE TISSUE PROTEINS; NEURAL PATHWAYS; NEURONS; SEXUAL BEHAVIOR, ANIMAL; TRANSCRIPTION FACTORS;

EID: 84897078689     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-014-0891-5     Document Type: Review

References (102)

1. Anand A, Villella A, Ryner LC, Carlo T, Goodwin SF, Song HJ, Gailey DA, Morales A, Hall C, Baker BS, Taylor BJ (2001) Molecular genetic dissection of the sex-specific and vital functions of the Drosophila melanogaster sex determination gene fruitless. Genetics 158: 1569-1595.
2. Bastock M, Manning A (1955) The courtship of Drosophila melanogaster. Behaviour 8: 85-111.
3. Bennet-Clark HC, Ewing AW (1968) The wing mechanism involved in the courtship of Drosophila. J Exp Biol 49: 117-128.
4. Billeter JC, Villella A, Allendorfer JB, Dornan AJ, Richardson M, Gailey DA, Goodwin SF (2006) Isoform-specific control of male neuronal differentiation and behavior in Drosophila by the fruitless gene. Curr Biol 16: 1063-1076.
5. Billeter JC, Atallah J, Krupp JJ, Millar JG, Levine JD (2009) Specialized cells tag sexual and species identity in Drosophilamelanogaster. Nature 461: 987-991.
6. Bocklandt S, Vilain E (2007) Sex differences in brain and behavior: hormones versus genes. Adv Genet 59: 245-266.
7. Bray S, Amrein H (2003) A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 39: 1019-1029.
8. Butterworth FM (1969) Lipids of Drosophila: a newly detected lipid in the male. Science 163: 1356-1357.
9. Cashero S, Ostrovsky AD, Yu JY, Dickson BJ, Jefferis GS (2010) Sexual dimorphism in the fly brain. Curr Biol 20: 1589-1601.
10. Chiang AS, Lin CY, Chuang CC, Chang HM, Hsieh CH, Yeh CW, Shih CT, Wu JJ, Wang GT, Chen YC, Wu CC, Chen GY, Ching YT, Lee PC, Lin CY, Lin HH, Wu CC, Hsu HW, Huang YA, Chen JY, Chiang HJ, Lu CF, Ni RF, Yeh CY, Hwang JK (2011) Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Curr Biol 21: 1-11.
11. Clyne JD, Miesenböck G (2008) Sex-specific control and tuning of the pattern generator for courtship song in Drosophila. Cell 133: 354-363.
12. Currie DA, Bate M (1995) Innervation is essential for the development and differentiation of a sex-specific adult muscle in Drosophila melanogaster. Development 121: 2549-2557.
13. Dalton JE, Lebo MS, Sanders LE, Sun F, Arbeitman MN (2009) Ecdysone receptor acts in fruitless-expressing neurons to mediate Drosophila courtship behaviors. Curr Biol 19: 1447-1452.
14. Datta SR, Vasconcelos ML, Ruta V, Luo S, Wong A, Demir E, Flores J, Balonze K, Dickson BJ, Axel R (2008) The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature 452: 473-477.
15. Demir E, Dickson BJ (2005) fruitless splicing specifies male courtship behavior in Drosophila. Cell 121: 785-794.
16. Eberl DF, Duyk GM, Perrimon NA (1997) Genetic screen for mutations that disrupt an auditory response in Drosophila melanogaster. Proc Natl Acad Sci USA 94: 14837-14842.
17. Ejima A, Griffith LC (2008) Courtship initiation is stimulated by acoustic signals in Drosophila melanogaster. PLoS ONE 3: e3246.
18. Everaerts C, Farine J, Cobb M, Ferveur J (2010) Drosophila cuticular hydrocarbons revisited: mating status alters cuticular profiles. PLoS ONE 5: e9607.
19. Ewing A (1978) The antenna of Drosophila as a 'love song' receptor. Physiol Entomol 3: 33-36.
20. Fen P, Manoli DS, Ahmed OM, Chen Y, Agarwal N, Kwong S, Cai AG, Neitz J, Rsnsio A, Baker BS, Shah NM (2013) Genetic and neural mechanisms that inhibit Drosophila from mating with other species. Cell 154: 89-102.
21. Gailey DA, Hall JC (1989) Behavior and cytogenetics of fruitless in Drosophila melanogaster: different courtship defects caused by separate, closely linked lesions. Genetics 121: 773-785.
22. Gailey DA, Taylor BJ, Hall JC (1991) Elements of the fruitless locus regulate development of the muscle of Lawrence, a male-specific structure in the abdomen of Drosophila melanogaster adults. Development 113: 879-890.
23. Gaj T, Gersbach CA, Barbas CF 3rd (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31: 397-405.
24. Gill KS (1963) A mutation causing abnormal courtship and mating behavior in males of Drosophila melanogaster. Am Zool 3: 507.
25. Goodwin SF, Taylor BJ, Villella A, Foss M, Ryner LC, Baker BS, Hall JC (2000) Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Genetics 154: 725-745.
26. Goto J, Mikawa Y, Koganezawa M, Ito H, Yamamoto D (2011) Sexually dimorphic shaping of interneuron dendrites involves the Hunchback transcription factor. J Neurosci 31: 5454-5459.
27. Greenspan RJ, Ferveur J (2000) Courtship in Drosophila. Annu Rev Genet 34: 205-232.
28. Grosjean Y, Rytz R, Farine JP, Abuin L, Cortot J, Jefferis GS, Benton R (2011) An olfactory receptor for food-derived odors promotes male courtship in Drosophila. Nature 478: 236-240.
29. Hall JC (1977) Portions of the central nervous system controlling reproductive behavior in Drosophila melanogaster. Behav Genet 7: 291-312.
30. Hall JC (1982) Genetics of the nervous system in Drosophila. Q Rev Biophys 15: 223-479.
31. Heinrichs V, Ryner LC, Baker BS (1998) Regulation of sex-specific selection of fruitless 5′ splice sites by transformer and transformer-2. Mol Cell Biol 18: 450-458.
32. Hildebrand JG (1996) Olfactory control of behavior in moths: central processing of odor information and the functional significance of olfactory glomeruli. J Comp Physiol A 178: 5-19.
33. Ito H, Fujitani K, Usui K, Shimizu-Nishikawa K, Tanaka S, Yamamoto D (1996) Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc Natl Acad Sci USA 93: 9687-9692.
34. Ito H, Sato K, Koganezawa M, Ote M, Matsumoto K, Hama C, Yamamoto D (2012) Fruitless recruits two antagonistic chromatin factors to establish single-neuron sexual dimorphism. Cell 149: 1327-1338.
35. Jallon JM (1984) A few chemical words exchanged by Drosophila during courtship and mating. Behav Genet 14: 441-478.
36. Jefferis GS, Potter CJ, Chan AM, Marin EC, Rohlfing T, Maurer CR Jr, Luo L (2007) Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128: 1187-1203.
37. Kamikouchi A, Inagaki HK, Effertz T, Hendrich O, Fiala A, Gopfert MC, Ito K (2009) The neural basis of Drosophila gravity-sensing and hearing. Nature 458: 165-171.
38. Kharchenko PV, Alekseyenko AA, Schwartz YB, Minoda A, Riddle NC, Ernst J, Sabo PJ, Larschan E, Gorchakov AA, Gu T, Linder-Basso D, Plachetka A, Shanower G, Tolstorukov MY, Luquette LJ, Xi R, Jung YL, Park RW, Bishop EP, Canfield TK, Sandstrom R, Thurman RE, MacAlpine DM, Stamatoyannopoulos JA, Kellis M, Elgin SC, Kuroda MI, Pirrotta V, Karpen GH, Park PJ (2010) Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471(7339): 480-485.
39. Kim WJ, Jan LY, Jan YN (2012) Contribution of visual and circadian neural circuits to memory for prolonged mating induced by rivals. Nat Neurosci 15: 876-883.
40. Kimura K (2011) Role of cell death in the formation of sexual dimorphism in the Drosophila central nervous system. Develop Growth Differ 53: 236-244.
41. Kimura K, Ote M, Tazawa T, Yamamoto D (2005) Fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain. Nature 438: 229-233.
42. Kimura K, Hachiya T, Koganezawa M, Tazawa T, Yamamoto D (2008) Fruitless and Doublesex coordinate to generate male-specific neurons that can initiate courtship. Neuron 59: 759-769.
43. Koganezawa M, Haba D, Matsuo T, Yamamoto D (2010) The shaping of male courtship posture by lateralized gustatory inputs to male-specific interneurons. Curr Biol 20: 1-8.
44. Kohatsu S, Koganezawa M, Yamamoto D (2011) Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron 69: 498-508.
45. Kohl J, Ostrovsky AD, Frechter S, Jefferis GSXE (2013) A bidirectional circuit switch reroutes pheromone signals in male and female brains. Cell 155: 1610-1623.
46. Kondoh Y, Kaneshiro KY, Kimura K, Yamamoto D (2003) Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila. Proc R Soc Lond B 270: 1005-1013.
47. Krstic D, Boll W, Noll M (2009) Sensory integration regulating male courtship behavior in Drosophila. PLoS ONE 4: e4457.
48. Kurtovic A, Widmer A, Dickson BJ (2007) A single class of olfactory neurons mediates behavioral responses to Drosophila sex pheromone. Nature 446: 542-546.
49. Lacaille F, Hiroi M, Twele R, Inoshita T, Umemoto D, Maniere G, Marion-Poll F, Ozaki M, Francke W, Cobb M, Everaerts C, Tanimura T, Ferveur JF (2007) An inhibitory sex pheromone tastes bitter for Drosophila males. PLoS ONE 8: e661.
50. Lam BJ, Bakshi A, Ekinci FY, Webb J, Graveley BR, Hertel KJ (2003) Enhancer-dependent 5′-splice site control of fruitless pre-mRNA splicing. J Biol Chem 278: 22740-22747.
51. Lawrence PA, Johnson P (1984) The genetic specification of pattern in a Drosophila muscle. Cell 36: 775-782.
52. Lawrence PA, Johnson P (1986) The muscle pattern of a segment of Drosophila may be determined by neurons and not by contribution myoblasts. Cell 45: 505-513.
53. Lee T, Luo L (1999) Mosaic analysis with a repressible neurotechnique cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 45-461.
54. Lee G, Foss M, Goodwin SF, Carlo T, Taylor BJ, Hall JC (2000) Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila central nervous system. J Neurobiol 15: 404-426.
55. Lee G, Hall JC, Park JH (2002) doublesex gene expression in the central nervous system of Drosophila melanogaster. J Neurogenet 16: 229-248.
56. Lin H, Mann KJ, Starostina E, Kinser RD, Pikilny CW (2005) A Drosophila DEG/ENaC channel subunit is required for male response to female pheromones. Proc Natl Acad Sci USA 102: 12831-12836.
57. Liu L, Ni JQ, Shi YD, Oakeley EJ, Sun FL (2005) Sex-specific role of Drosophila melanogaster HP1 regulating chromatin structure and gene transcription. Nat Genet 37: 1361-1366.
58. Liu T, Starostina E, Vijayan V, Pikielny CW (2012) Two Drosophila DEG/ENaC channel subunits have distinct functions in gustatory that active male courtship. J Neurosci 32: 11879-11889.
59. Lu B, LaMora A, Sun Y, Welsh MJ, Ben-Shahar Y (2012) ppk23-Dependent chemosensory functions contribute to courtship behavior in Drosophila melanogaster. PLoS Genet 8: e1002587.
60. Luo L, Callaway EM, Svoboda K (2008) Genetic dissection of neural circuits. Neuron 57: 634-660.
61. Manoli DS, Foss M, Villella A, Taylor BJ, Hall JC, Baker BS (2005) Male-specific fruitless specifies the neural substrates of Drosophila courtship behavior. Nature 436: 395-400.
62. Mellert DJ, Knapp J, Manoli DS, Meissner GW, Baker BS (2010) Midline crossing by gustatory receptor neuron axons is regulated by Fruitless, Doublesex and Roundabout receptors. Development 137: 323-332.
63. Miyamoto T, Amrein H (2008) Suppression of male courtship by a Drosophila pheromone receptor. Nat Neurosci 11: 874-876.
64. Moon SJ, Lee Y, Jiao Y, Montell CA (2009) Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr Biol 19: 1623-1627.
65. Nagoshi RN, McKeown M, Burtis KC, Belote JM, Baker BS (1988) The control of alternative splicing at genes regulating sexual differentiation in D. melanogaster. Cell 53: 229-236.
66. Nielsen AL, Ortiz JA, You J, Oulad-Abdelghani M, Khechumian R, Gansmuller A, Chambon P, Losson R (1999) Interaction with members of the heterochromatin protein 1 (HP1) family and histone deacetylation are differentially involved in transcriptional silencing by members of the TLF1 family. EMBO J 18: 6385-6395.
67. Nojima T, Kimura K, Koganezawa M, Yamamoto D (2010) Neuronal synaptic outputs determine the sexual fate of postsynaptic targets. Curr Biol 20: 836-840.
68. Pan Y, Robinett CC, Baker BS (2011) Turning males on: activation of male courtship behavior in Drosophila melanogaster. PLoS ONE 6: e21144.
69. Pan Y, Messner GW, Baker BS (2012) Joint control of Drosophila male courtship behavior by motion cues and activation of male-specific P1 neurons. Proc Natl Acad Sci USA 109: 10065-10070.
70. Piacentini L, Fanti L, Berloco M, Perrini B, Pimpinelli S (2003) Heterochromatin protein (HP1) is associated with induced gene expression in Drosophila euchromatin. J Cell Biol 161: 707-714.
71. Possidente DR, Murphey RK (1989) Genetic control of sexually dimorphic axon morphology in Drosophila sensory neurons. Dev Biol 132: 448-457.
72. Rideout EJ, Billeter J, Goodwin SF (2007) The sex-determination genes fruitless and doublesex specify a neural substrate required for courtship song. Curr Biol 17: 1473-1478.
73. Rideout EJ, Dornan AJ, Neville MC, Eadie S, Goodwin SF (2010) Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nat Neurosci 13: 458-466.
74. Robinett CC, Vaughan AG, Knapp J, Baker BS (2010) Sex and the single cell. II. There is a time and place for sex. PLoS ONE 8: e1000365.
75. Rubinstein CD, Rivlin PK, Hoy RR (2010) Genetic feminization of the thoracic nervous system disrupts courtship song in male Drosophila melanogaster. J Neurogenet 24: 234-245.
76. Ruta V, Datta SR, Vasconcelos ML, Freeland J, Looger LL, Axel R (2010) A dimorphic pheromone circuit in Drosophila from sensory input descending output. Nature 468: 686-690.
77. Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, Hall JC, Taylor BJ, Wasserman SA (1996) Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87: 1079-1089.
78. Sakai T, Isono K, Tomaru M, Oguma Y (1997) Light-affected male following behavior is involved in light-dependent mating in Drosophila melanogaster. Genes Genet Syst 72: 275-281.
79. Salz HK (2011) Sex determination in insects: a binary decision based on alternative splicing. Curr Opin Genet Dev 21: 395-400.
80. Sanders LE, Arbeitman MN (2008) Doublesex establishes sexual dimorphism in the Drosophila central nervous system in an isoform-dependent manner by directing cell number. Dev Biol 132: 448-457.
81. Schreiber SL, Bernstein BE (2002) Signaling network model of chromatin. Cell 111: 771-778.
82. Sekido R, Lovell-Badge R (2009) Sex determination and SRY: down to a wink and a nudge? Trends Genet 25: 19-29.
83. Shirangi TR, Taylor BJ, McKeown M (2006) A double-switch system regulates male courtship behavior in male and female Drosophila melanogaster. Nat Genet 38: 1435-1439.
84. Song HJ, Billeter JC, Reynaud E, Carlo T, Spana EP, Perrimon N, Goodwin SF, Baker BS, Taylor BJ (2002) The fruitless gene is required for the proper formation of axonal tracts in the embryonic central nervous system of Drosophila. Genetics 162: 1703-1724.
85. Starostina E, Liu T, Vijayan V, Zheng Z, Siwicki KK, Pikielny CW (2012) A Drosophila DEG/ENaC subunit functions specifically in gustatory neurons required for male courtship behavior. J Neurosci 32: 4665-4674.
86. Stockinger P, Kvitsiani D, Rotkopf S, Tirián L, Dickson BJ (2005) Neural circuitry that governs Drosophila male courtship behavior. Cell 121: 795-807.
87. Taylor BJ (1992) Differentiation of a male-specific muscle in Drosophila melanogaster does not require the sex-determining genes doublesex or intersex. Genetics 132: 179-191.
88. Taylor BJ, Knittel LM (1995) Sex-specific differentiation of a male-specific abdominal muscle, the Muscle of Lawrence, is abnormal in hydroxyurea-treated and in fruitless male flies. Development 121: 3079-3088.
89. Taylor BJ, Villella A, Ryner LC, Baker BS, Hall JC (1994) Behavioral and neurobiological implications of sex-determining factors in Drosophila. Dev Genet 15: 275-296.
90. The modENCODE Consortium (2010) Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 330: 1787-1796.
91. Thistle R, Cameron P, Ghorayshi A, Dennison L, Scott K (2012) Contact chemoreceptors mediate male-male repulsion male-female attraction during Drosophila courtship. Cell 149: 1140-1151.
92. Toda H, Zhao X, Dickson BJ (2012) The Drosophila female aphrodisiac pheromone actives ppk23 + sensory neurons to elicit male courtship behavior. Cell Rep 1: 599-607.
93. Tootoonian S, Coen P, Kawai R, Murthy M (2012) Neural representations of courtship song in the Drosophila brain. J Neurosci 32: 787-798.
94. Usui-Aoki K, Ito H, Ui-Tei K, Takahashi K, Lukacsovich T, Awano W, Nakata H, Piao ZF, Nilsson EE, Tomida J, Yamamoto D (2000) Formation of the male-specific muscle in female Drosophila by ectopic fruitless expression. Nat Cell Biol 2: 500-506.
95. Venken KJT, Simpson JH, Bellen HJ (2011) Genetic manipulation of genes and cells in the nervous system of the fruit fly. Neuron 72: 202-230.
96. von Philipsborn AC, Liu T, Yu JY, Masser C, Bidaye SS, Dickson BJ (2011) Neuronal control of Drosophila courtship song. Neuron 69: 509-522.
97. von Schilcher F (1976a) The function of pulse song and sine song in the courtship of Drosophila melanogaster. Anim Behav 24: 622-625.
98. von Schilcher F (1976b) The role of auditory stimuli in the courtship of Drosophila melanogaster. Anim Behav 24: 18-26.
99. Watanabe K, Toba G, Koganezawa M, Yamamoto D (2011) Gr39a, a highly diversified gustatory receptor in Drosophila, has a role in sexual behavior. Behav Genet 41: 746-753.
100. Yamamoto D, Ishikawa Y (2013) Genetic and neural bases for species-specific behavior in Drosophila species. J Neurogenet. doi: 10. 3109/01677063. 2013. 800060.
101. Yew JY, Dreisewerd K, Luftmann H, Muthing J, Pohlentz G, Kravitz EA (2009) A new male sex pheromone and cuticular cues for chemical communication in Drosophila. Curr Biol 19: 1245-1254.
102. Yu JY, Kanai MI, Demir E, Jefferis GS, Dickson BJ (2010) Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr Biol 20: 1602-1614.